56 Ornitología Colombiana No. 9 (2010): 56-70
A NEW SPECIES OF ANTPITTA (GRALLARIIDAE: GRALLARIA) FROM THE NORTHERN SECTOR OF THE WESTERN ANDES OF COLOMBIA
Una especie nueva de tororoi (Grallariidae: Grallaria) del sector norte de la Cordillera Occidental de los Andes colombianos
Diego Carantón-Ayala1 Fundacion ProAves, Cra. 20 # 36-61, Bogotá, Colombia. Grupo de Observadores de Aves del Tolima GOAT, Facultad de Ciencias, Universidad del Tolima, Ibagué, Colombia. [email protected]
Katherine Certuche-Cubillos Programa de Biología, Facultad de Ciencias, Universidad del Tolima, Ibagué, Colombia. [email protected] ABSTRACT
We describe the Urrao Antpitta (Grallariidae: Grallaria urraoensis), a new species of suboscine passerine endemic to high Andean forests below Páramo de Frontino, in the northern sector of the Western Andes of Colombia. The new species is similar to the Brown-banded Antpitta (Grallaria milleri) from the Central Andes, but differs from it vocally and in its slightly larger size, lack of pectoral band, duller brown-olive coloration in the upperparts, uniform light gray underparts, and whitish lores. The new species occurs in the undergrowth of primary and secondary cloud forests dominated by Chusquea bamboo at elevations between 2500-3200 m at the type locality. We present notes on the ecology, distribution, behavior, reproductive biology, vocalizations, and conservation of the new species. The montane forests in the northern sector of the Western Andes to which the Urrao Antpitta is endemic are threatened by deforestation, fragmentation, and mining. These factors, in combination with the restricted geographic and ecological distribution of the new species, make it an important priority for conservation action.
Key words: Colombia, Grallaria urraoensis, high Andean forest, new species, Western Andes.
RESUMEN
Describimos al Tororoi de Urrao (Grallariidae: Grallaria urraoensis), una nueva especie de passeriforme suboscino endémica de los bosques altoandinos del Páramo de Frontino, sector norte de la Cordillera Occidental de los Andes de Colombia. La nueva especie es similar al Tororoi de Miller (Grallaria milleri) de la Cordillera Central, pero difiere de esta especie en sus vocalizaciones y por ser ligeramente más grande, sin banda pectoral, con coloración café-oliva más opaca por encima, gris claro uniforme en las partes inferiores y bridas blanquecinas. La nueva especie se encuentra en el sotobosque de bosques nublados primarios y secundarios dominado por bambúes del género Chusquea entre elevaciones de 2500 a 3200 m en la localidad tipo. Presentamos anotaciones sobre la ecología, distribución, comportamiento, reproducción, vocalizaciones y conservación de esta nueva especie. Los bosques de montaña del norte de la Cordillera Occidental donde se encuentra el Tororoi de Urrao están amenazados debido a deforestación, fragmentación y exploración minera. Estos factores, junto con la distribución geográfica y ecológica restringida de la nueva especie, hacen altamente prioritarios esfuerzos para su conservación.
Palabras clave: Bosque altoandino, Colombia, Cordillera Occidental, Grallaria urraoensis, nueva especie. 1Present address: Grupo de Observadores de Aves del Tolima GOAT, Facultad de Ciencias, Universidad del Tolima, Ibagué, Colombia. Ornitología Colombiana No. 9 (2010) 57
INTRODUCTION the diversity and distributions of birds in the northern sector of the Western Andes (Cuervo et al. The antpittas (family Grallariidae) are terrestrial 2003, Krabbe et al. 2006, Pulgarín-R. & Múnera-P. Neotropical passerine birds of the dense understory 2006), ornithological explorations in the area of humid forests, scrublands, and alpine habitats remain sparse. More generally, the avifauna of this with scattered bushes in the high Andes. Because of cordillera as a whole remains insufficently their retiring habitats, antpittas are difficult to documented, as evidenced by several new records observe and collect, and information on most implying significant range extensions for multiple aspects of their biology is scarce (Krabbe & species (Cuervo et al. 2003), and especially by the Schulenberg 2003; Greeney et al. 2008). The group recent discovery of four species new to science reaches its highest diversity in the tropical Andes, (Salaman & Stiles 1996; Robbins & Stiles 1999; especially above 800 m, where many species have Salaman et al. 2003; Cortés-Diago et al. 2007) and restricted geographic distributions (Krabbe & the rediscovery of two more (Toro & Flórez 2001; Schulenberg 2003). Owing to habitat destruction Krabbe et al. 2005). Five species of birds are and to their small geographic ranges, several species endemic to this mountain range: Gorgeted Puffleg of antpittas are threatened with extinction (Renjifo (Eriocnemis isabellae), Colorful Puffleg (E. et al. 2002), although part of their apparent rarity mirabilis), Dusky Starfrontlet (Coeligena orina), might actually reflect insufficient information Munchique Wood-Wren (Henicorhina negreti), and regarding their distribution and ecology (Kattan & Chestnut-bellied Flowerpiercer (Diglossa Beltrán 1997; Krabbe & Coopmans 2000). With gloriossisima). All occur above 2200 m, exhibit increasing knowledge of the vocalizations of highly localized distributions, and are considered Neotropical birds, in combination with expeditions threatened with extinction (Salaman et al. 2002; to several previously unexplored sites over the past Toro 2002; Salaman et al. 2003; Krabbe et al. 2005; decades, a significant number of species of antpittas Cortés-Diago et al. 2007). have been recently described, especially in the genus Grallaria (Lowery & O'Neill 1969; A recent survey by an Evaluation of Biodiversity of Schulenberg & Williams 1982; Graves 1987; Stiles the Andes Expedition (EBA) team to the Páramo de 1992; Krabbe et al. 1999). In this paper, we Frontino (also known as Páramo del Sol or Páramo document the existence of yet another previously de Urrao) in Dept. Antioquia (Flórez et al. 2004) led unknown species in this genus from the Cordillera to the rediscovery of the Dusky Starfrontlet Occidental of the Colombian Andes. (Coeligena orina) and revealed the existence of populations of other rare and threatened bird species The Western Andes are, on average, the lowest of in this part of the northern Western Andes (Krabbe the three ranges of the Colombian Andes et al. 2005, 2006). Thus, with the goal of protecting (Hernández-Camacho 1992). Only seven peaks habitat for threatened species in the area, Fundación along the ca. 1200 km length of this range reach ProAves promoted the establishment of the Reserva sufficient elevations to support paramo habitats; Natural Colibrí del Sol in the municipality of Urrao, because the cordillera is much lower in many areas, Antioquia (Fundación ProAves 2009). these high-elevation habitats are highly isolated (Krabbe et al. 2006). The most extensive areas During regular monitoring activities conducted on covered by paramo vegetation occur in the northern 27 September 2007 at 2780 m elevation in a forest sector, in the departments of Chocó and Antioquia. near Páramo de Frontino, DCA captured an unsual These areas have received relatively little attention antpitta in the genus Grallaria that was examined, from ornithologists. In fact, most of the earlier measured, and released. This individual could not be expeditions to montane areas of the department of photographed, but it clearly did not match any of the Antioquia focused on the Central Andes (around species of antpitta known to occur in the area. A the city of Medellín), whereas studies in the second individual was captured, measured, exam- Western Andes concentrated on its southern sector ined, photographed, and released on 5 February (reviewed by Cuervo et al. 2003, 2008). Although 2008 within the same forest, some 400 m from the recent studies have increased our understanding of site of the first capture. On 20 February 2008, DCA 58 New species of Grallaria from Colombia Carantón-Ayala & Certuche-Cubillos set mist nets in the same forest in order to capture Diagnosis.- A medium-sized antpitta (ca. 57 g), the then mysterious Grallaria, but owing to heavy assigned to the genus Grallaria based on its typical rains was unable to operate them. However, when shape and proportions, strong bill markedly curved opening the nets on the morning of 21 February, a from the base, conspicuous rictal bristles, short and dead bird was found hanging from one of them; rounded wings, long tarsi, short tail, 2-notched apparently one of its feet got entangled after it sternum, distinctive tarsal scutellation, and perched on the closed net. Serendipitously, this terrestrial habits. It can be distinguished from other individual turned out to be an antpitta matching the species in the genus by its combination of two main ones observed and captured earlier at the site. DCA colors, brown-olive above and gray below. The new and KCC prepared the specimen and compared it species is similar to G. milleri, probably its closest with those of other species in the genus deposited in relative, but can be diagnosed based on the the ornithological collections of the Instituto de combination of (1) plumage characters: the new Investigación de Recursos Biológicos Alexander species has a more olivaceous dorsum, a brownish- von Humboldt (IAvH), Instituto de Ciencias olive throat (whitish in G. milleri), and lacks a Naturales at Universidad Nacional de Colombia brown pectoral band and contrasting whitish (ICN-MHN), and Universidad del Valle (UVC), abdomen (Fig. 1); (2) its heavier bill, greater body confirming its phenotypic distinctiveness. The mass and probably longer wing and tail (see below); specimen appeared to be most similar to, although and (3) its different vocalizations (see below). appreciably distinct from, the Brown-banded Antpitta (Grallaria milleri), a species endemic to Description of holotype.- Color nomenclature the Central Andes. On 30 March 2008, another follows Smithe (1975, 1981). A fairly small, clearly individual was captured and collected. bicolored Grallaria antpitta. Forehead, crown, nape, Subsequently, DCA and KCC obtained recordings back, scapular area, and rump uniformly dull brown of the song and calls of this antpitta, which allowed -olive (Raw Umber 123); rectrices darker (between locating additional individuals in other properties in Mars Brown 223A and Prout's Brown 121A). Lores the area of Páramo de Frontino, to clarify their close to Cream Color 54, inconspicuous buffy elevational distribution and habitat use, and to study eyering with feathers tipped black, auriculars their behavior. At that time, the possibility that this generally Mars Brown 223A, but middle section of antpitta might represent an undescribed species feathers close to Ochraceous Tawny 123B and tips began to be considered. darker. Middle and upper secondary coverts and external margin of primary coverts Raw Umber, Following additional comparisons at museums and internal margin of primary coverts dark gray; detailed analyses of vocalizations, it became clear primaries proximally close to Vandyke Brown 221 that the antpitta found at Urrao is indeed an and distally dull brown-olive (123); secondaries 6 undescribed species, which we propose to name: and 7, which were retained, somewhat darker (close to 223A); interior wing coverts between Cinnamon Grallaria urraoensis, sp. nov. Rufous 40 and Tawny 38. Throat feathers light gray Urrao Antpitta (between Neutral Gray 82 and Medium Neutral Tororoi de Urrao Gray 84) and tipped dull brown-olive (123), producing a mottled appearance; sides of throat 123. Holotype.- Adult male (80% skull ossification) Breast and sides of breast pale gray (between prepared as a study skin and deposited (catalogue Glaucus 78 and 80), with feathers narrowly tipped no. 36689) in the ornithological collection of the grayish white (close to Smoke Gray 44); center of Instituto de Ciencias Naturales, Universidad abdomen dull White (between Cream Color 54 y Nacional de Colombia (ICN-MHN), Bogotá. Pale Horn Color 92), thighs olive brownish (Olive Collected 30 March 2008 by DCA and prepared by Brown 28). Iris dark brown, maxilla black and KCC at the Reserva Natural Colibrí del Sol, south mandible horn, with tomia and tip lighter; tarsi and of Páramo de Frontino, vereda El Chuscal, ca. 17 feet blue- gray. An adult male (no bursa, skull km north of the town of Urrao, department of ossification 80%) in breeding condition (large Antioquia, Colombia (2850 m; 6º26’N, 76º05’W). cloacal protuberance, brood patch, well developed Ornitología Colombiana No. 9 (2010) 59
A. B.
C. D.
Figure 1. Specimens of the Brown-banded antpitta (Grallaria milleri) (left) and the Urrao Antpitta (Grallaria urraoensis sp. nov.) (center holotype and right paratype). A. ventral view, B. dorsal view, C. lateral view and D. lateral view of upper parts (left G. milleri and right G. urraoensis). Note differences in size, throat pattern, breast pattern and abdomen coloration. testes: left 14.4 x 8.7 mm, right 13.5 x 8.6 mm), mainly coleopteran remains. with no subcutaneous fat. Finishing complete molt; all primaries had been replaced except for primary Paratype.- A likely immature male (30% skull 10 in the left wing, which was emerging from ossification, but enlarged gonads: left testis 13.2 x sheath; secondaries 1-5, 8, and 9 replaced, 6 and 7 6.5 mm, right 14.6 x 6.8 mm), catalogue no. 36688 retained. Stomach contents: insects, including in the ornithological collection at the ICN-MHN. 60 New species of Grallaria from Colombia Carantón-Ayala & Certuche-Cubillos
0.02 0.02 0.01 0.01 wing Ratio Ratio 0.50 ± ± 0.50 0.47 ± ± 0.47 tarsus/ tarsus/
0 tail 0.04 0.04 Ratio Ratio 0.79 ± ± 0.79 0.89 ± ± 0.89
tarsus/
tail/ 0.04 0.04 0.02 0.02 wing Ratio Ratio G. milleri. G. 0.63 ± ± 0.63 0.52 ± ± 0.52 and
(g) 2.93 2.93 0.71 0.71 mass Body 51.3 ± 51.3 ± 56.9 ± 56.9 ±
1.87 1.87 1.34 1.34 (mm) 44.3 ± 44.3 ± length 45.5 ± 45.5 Tarsus Grallaria urraoensis
Tail 2.68 2.68 0.14 0.14 56.1 ± 56.1 ± 63.1 ± 63.1 ± length
2.72 2.72 0.78 0.78 (mm) Wing chord 88.8 ± 88.8 ± 95.9 ± 95.9 ±
Bill 0.26 0.26 0.07 0.07 6.9 ± 6.9 (mm) height height d standard deviations in mm) of in deviations d standard
0.28 0.28 13.2 ± 13.2 ± 11.3 ±1.17 ±1.17 11.3 ± 6.7 width (mm) Commissure Commissure
0.95 0.95 0.92 0.92 Total (mm) 22.5 ± 22.5 ± 22.8 ± 22.8 ± culmen
- - 22.2 12.5 - 0.49 0.72 0.67 42.7 55 6.7 21.4 58.8 87 12.2 0.52 0.81 0.64 47.1 51 6.7 57.7 89 . Morphological measurements (means an 20.0 20.0 21.5 12.5 20.4 22.2 6.4 45.0 55.5 87.5 54 10.1 0.51 0.81 0.63 21.4 23.9 6.7 87 10.6 0.51 0.83 0.61 50.5 44.1 53.4 6.9 90 0.52 0.82 0.63 53.5 47.0 57.1 20.4 20.4 23.5 13.4 18.9 22.2 7.0 0.48 0.89 0.54 56.4 46.5 63.0 95.4 13.0 6.9 0.46 0.89 0.51 57.4 44.6 63.2 96.5 1.06 21.0 21.0 23.8 13.0 0.52 0.75 0.70 44.8 46 7.2 59.7 85 18.1 18.1 23.5 10.7 20.0 22.1 6.3 10.5 41.8 51.8 88.5 0.47 53 0.81 0.47 0.81 0.59 20.5 0.58 43.9 48 6.7 22.6 53.9 93 10.1 0.46 0.74 0.62 42.5 51 6.7 57.7 93 ±1.06 (mm) culmen Exposed
Table 1
UVC 6181 Male UVC 6171 Male UVC 6178 Female x ± SD 20.2 Grallaria Grallaria urraoensis ICN 36689 Male (Holotype) ICN 36688 Male (Paratype) ± SD x ± 19.6 ICN 36692 Female IAvH 13203 Female IAVH 13205 Male UVC 6180 Male UVC 6179 Male UVC 6182 Male Grallaria milleri Ornitología Colombiana No. 9 (2010) 61
Collected at the Páramo de Frontino along a forest flanks. edge covered by Chusquea bamboo at 2820 m elevation on 20 February 2008. Specimen with no The paratype is generally very similar to the subcutaneous fat; stomach contained insect holotype, the main difference being that the former fragments; moderate body molt, with sheaths in the exhibits darker brown (i.e. Mars Brown 223A) in Table 2. Field measurements of individuals not collected of G urraoensis. Adult 1 Adult 2 Adult 3 Juvenile Mean Fledgling
Exposed culmen (mm) 20.4 20.5 20.2 18.8 20.0 - Total culmen (mm) 23.0 23.3 23.3 21.0 22.7 16.0 Commissure width (mm) 15.0 14.6 12.8 15.3 14.4 16.8 Bill height (mm) 6.8 7 7.2 7.1 7.0 5.1 Wing chord (mm) 90 89 87 90 89.0 51.6 Tail length 56.3 58.4 55.5 60.5 57.7 - Tarsus length (mm) 46.3 45.8 44.7 44.1 45.2 31.2 Body mass (g) 56.9 66.4 59.8 55.4 59.6 41.1 Ratio tail/wing 0.62 0.65 0.63 0.67 0.64 - Ratio tarsus/tail 0.82 0.78 0.80 0.72 0.78 - Ratio tarsus/wing 0.51 0.51 0.51 0.49 0.50 -
A. B.
C. D.
Figure 2. Individuals of Urrao Antpitta (Grallaria urraoensis) of different ages: (A) nestling, (B) juvenile, and (C and D) adult. 62 New species of Grallaria from Colombia Carantón-Ayala & Certuche-Cubillos the primaries, secondaries, primary coverts, the combined. However, this might be due to differing most external secondary coverts and some scattered techniques under the two situations; the wing and feathers on the head and back, breast darker gray. tail lengths of the two specimens of G. urraoensis These differences might be related to age, because are considerably greater than measurements of all the paratype is likely a younger male as suggested specimens of G. m. milleri, more concordant with its by cranial ossification. Morphometric variation is greater mass. The recently-described G. m. gilesi slight (Table 1, Fig. 1). (Salaman et al. 2009) is larger than the nominate in most measurements but has a much shorter bill and Additional individuals examined.- Four individuals tarsus; it differs from G. urraoensis in these of the new species have been captured, examined, measurements as well. measured, banded, and released in the Páramo de Frontino area, including three adults and one Vocalizations .- As with other members of the juvenile; we also photographed a fledgling (Table 2, genus Grallaria (Krabbe & Schulenberg 2003), G. Fig. 2). Little variation in plumage pattern and urraoensis has distinctive vocalizations, which are coloration was observed among the adults; given from low perches in dense forest understory, assuming our sample included individuals of both often from within Chusquea thickets. Vocal activity sexes, the species is likely sexually monomorphic as is most frequent at dawn and dusk, but vocalizations are other antpittas. The juvenile had an overall can be heard throughout the day, especially under scaled appearance, with patches of black down with rainy and overcast conditions. The vocalizations of chestnut tips in most of the crown, nape, and flanks, G. urraoensis are similar to those of G. milleri and and in small patches in the scapular area, the rump of G. kaestneri (Cundinamarca Antpitta), two and the breast. Its belly was buff-colored, and the closely related species (see below), but differ from feathers on the sides of the throat were dark, giving them in several ways. it a blackish appearance. The maxilla was black proximally and orange distally, whereas the The territorial loudsong of G. urraoensis is the most mandible was entirely orange; bill commissures frequently heard vocalization, particularly from were conspicuously red-orange. The fledgling was February to April, presumably the beginning of the covered by a dense blackish down with brown edges breeding season; singing activity is reduced on the upperparts; these edges were wider and more substantially from June through August. The brightly colored in the lower back and rump. The loudsong (Fig. 3a) is, on average, 0.9 s long (SD ± belly, flanks, and lower part of the chest were 0.06 s, n=30), and is composed of three similarly largely buff, its feet were colored dark pink, and its shaped, high-pitched notes. The first and second bill was similar to that of the juvenile. Primaries and notes are relatively brief (0.13 ± 0.02 s and 0.14 ± secondaries had emerged c. 4 mm from their 0.02 s, respectively), whereas the third is somewhat sheaths, but rectrices had not yet started to appear. longer (0.18 ± 0.04 s); the interval between the first and second note is 0.30 ± 0.03 s, and that between REMARKS the second and third only 0.07 ± 0.02 s. Pitch (i.e. dominant frequency) also increases as the song Biometrics.- Combining the field-measured birds progresses: first note 2.93 ± 0.11 kHz, second note (Table 2) with measurements in the museum (Table 3.08 ± 0.10 kHz, third note 3.27 ± 0.10 kHz. The 1), G. urraoensis differs significantly from G. m. song of G. milleri (Fig. 3b) is similar but longer milleri (Mann-Whitney U tests) in having a taller (1.19 ± 0.16 s SD, n=20), and each of its individual bill (p<0.05) and a wider commissure (p<0.002) as notes is also longer (first 0.25±0.05 s, second well as a greater body mass (p<0.001), but not in 0.26±0.02 s, third 0.30±0.06 s) and differs in shape exposed or total culmen length or tarsus length. from those of G. urraoensis. The frequency range of Because our field measurements of wing and tail are each note, however, is similar to that in the song of smaller than the museum measurements, G. G. urraoensis. The dominant frequency is: first note urraoensis does not differ from G. m. milleri when 2.65 ± 0.12 kHz; second note 2.81 ± 0.11 kHz and field and museum measurements of the former are difference in the songs of the two species is Ornitología Colombiana No. 9 (2010) 63
8 8 A. A. 7 7
6 6
5 5
4 4 Frequency (kHz) (kHz) Frequency (kHz) Frequency 3 3
2 2
1 1
0 0 0.2 1.2 0.2 0.4 0.6 0.8 1.0 1.2 1.4 0.4 0.6 0.8 1.0 1.4 Time (s) Time (s) 8 8 B. B. 7 7
6 6
5 5
4 4 Frequency (kHz) (kHz) Frequency Frequency (kHz) (kHz) Frequency 3 3
2 2
1 1
0 0 0.2 0.4 0.6 0.8 1.0 1.2 1.4 0.2 0.4 0.6 0.8 1.0 1.2 1.4 Time (s) Time (s) 8 8 C. C. 7 7
6 6
5 5
4 4 Frequency (kHz) (kHz) Frequency Frequency (kHz) (kHz) Frequency 3 3
2 2
1 1
0 0 0.2 0.4 0.6 0.8 1.0 1.2 1.4 0.2 0.4 0.6 0.8 1.0 1.2 1.4 Time (s) Time (s) Figure 3. Songs of Andean antpittas: A. Urrao Antpitta Figure 4. Calls of Andean antpittas: A. Urrao Antpitta (Grallaria urraoensis), B. Brown-banded Antpitta (G. mil- (Grallaria urraoensis), B. Brown-banded Antpitta (G. mil- leri), and C. Cundinamarca Antpitta (G. kaestneri). leri), and C. Cundinamarca Antpitta (G. kaestneri).
64 New species of Grallaria from Colombia Carantón-Ayala & Certuche-Cubillos duration of the pause between the second and third similar elevations in the geographically isolated note; this pause is short and occasionally Cordillera Central of Colombia. G. urraoensis is imperceptible in G. milleri. diagnosable from all described forms of Grallaria in plumage color and voice, and is clearly at least a A second type of vocalization recorded from G. phylogenetic species (Cracraft 1989). These urraoensis is a short, loud call emitted in aggressive differences are comparable to those between related contexts (e.g. after song playbacks or after imitating species such as G. kaestneri, G. bangsi and G. its song), in response to loud noises, and during the milleri (which are also different genetically; C.D. nonbreeding season. This call (Fig. 4a) is louder and Cadena, unpubl. data), such that G. urraoensis higher-pitched than the song, and consists of a qualifies as a species under the biological species single wave-shaped note (~) that lasts for 0.31 ± concept (Johnson et al. 1999) as well. Referring to 0.03 s (n=11), beginning at 5.39 ± 0.17 kHz, then urraoensis, Salaman et al. (2009) stated that “it may descending to 4.94 ± 0.15 kHz, and rising again to be closer related to G. m. gilesi than to G. m. 5.19 ± 0.21 kHz (n= 11). The call of G. milleri milleri” because of its larger size and greater (Fig. 4b) differs in being longer (0.45 ± 0.09 s, geographical proximity (but in a different mountain n=21), U-shaped, and generally higher-pitched: it range). However, in plumage color and pattern, and begins at 6.31 ± 0.45 kHz, then descends to 5.09 ± bill and tarsus lengths we see no approach between 0.23 kHz, and rises at the end to 5.40 ± 0.18 kHz. gilesi and urraoensis (if anything, gilesi differs The call of G. kaestneri (Fig. 6c) has a rather more from urraoensis than does nominate milleri in different shape; it begins at 5.8-6.0 kHz, drops these features). Therefore, in the absence of genetic abruptly to 5.0 kHz. evidence, the statement by Salaman et al. (2009) on the affinities of urraoensis is unsupported. The similarity among the songs of the species most similar to G. urraoensis (G. milleri and G. Based on morphological and vocal similarities, we kaestneri) resides in the number of notes and the suggest that G. urraoensis, G. milleri, and G. ranges of frequencies, showing a general pattern of kaestneri, three species endemic to Colombia, three notes or whistles that increase gradually in probably form a clade. Based on plumage and their duration and frequency with each successive vocalizations (Stiles 1992), we suspect that another note slightly longer and higher-pitched. This song Colombian endemic, the Santa Marta Antpitta (G. model probably reflects a close phylogenetic bangsi ), may be a close relative of this clade. We affinity among these species. cannot address Chapman's (1912) hypothesis that G. erythrotis is a close relative of G. milleri and hence, Etymology.- The species names refer to the of G. urraoensis, although this appears unlikely on municipality where G. urraoensis was discovered geographic grounds. The hypothesized close and to which it may be restricted: Urrao, Dept. relationship of G. urraoensis with G. milleri is Antioquia, Colombia. The word Urrao is of consistent with results of phylogenetic (Cuervo et indigenous origin; these areas were originally al. 2005), phylogeographic (Cadena et al. 2007; occupied by a number of indigenous tribes, some Puebla-Olivares et al. 2008), and biogeographic currently represented by groups of the Embera- (Cuervo et al. 2008) studies indicating close Katío culture. affinities between species and populations of other bird groups occurring in the Western and Central Taxonomic affinities.- Within the subgenera of Andes of Colombia. Grallaria defined by Lowery & O'Neill (1969), the new species is referable to Oropezus owing to its Ecology and behavior.- Like other antpittas, G. tarsal scutellation, number of rectrices (12), uniform urraoensis is shy and inconspicuous, and thus plumage coloration in the upperparts and underparts difficult to observe even after playback; it is much lacking barring or streaking, and proportions more often heard than seen. However, it is locally between tail, wing, and tarsus length (Table 1). common at the area (especially between 2650 and Within Oropezus, G. urraoensis is phenotypically 2900 m elevation), where we have accumulated c. most similar to G. milleri, which is restricted to 70 observations and ca. 55 sound recordings, and Ornitología Colombiana No. 9 (2010) 65 we captured eight individuals between 2008 and breeding condition. In addition, vocal activity was October 2009. These encounters have taken place pronounced between February and May; also, we especially around Quebrada Santa Bárbara and El observed a fledgling on 12 June 2008 and captured 15, El Oso, and La Ilusión farms in the southeast of an adult with an old brood patch in June as well. Páramo de Frontino, where field activities have Thus, the breeding season may begin as early as intensified. The species is usually encountered in January and extend through several months; this pairs, although we often found single individuals as coincides with the dry first months of the year and well and on one occasion we recorded three with the breeding seasons of several other bird individuals in close proximity. The birds invariably species in the area. The fledgling we observed was remain on or close to the ground, where they move being fed by two adults that delivered mostly about dense bamboo vegetation and moss-covered earthworms; biparental feeding of nestlings (and substrates. Intense vocal activity during the first mostly with earthworms) seems to be general across months of 2008 and 2009 allowed us to conduct a species of Grallaria (Greeney et al. 2008). In preliminary assessment of population density at the addition, as observed in other antpittas (Greeney et type locality. Along a 1.5 km transect, we detected al. 2008), the fledgling appeared to be five territories defended by males, at least two of underdeveloped in comparison to fledglings of other which were paired. passerine species and its plumage was very different from that of the adults (see description above). Five additional species of antpitta have been recorded at the type locality of G. urraoensis: Habitat and distribution.- All individuals of G. Undulated (G. squamigera), Rufous (G. rufula), urraoensis captured, observed, or heard vocalizing Chestnut-naped (G. nuchalis), Chestnut-capped (G. at the Páramo de Frontino (Páramo del Sol) were ruficapilla), and Slate-crowned (Grallaricula nana). restricted to montane forests between 2500 and The Chestnut-naped Antpitta is the most common, 3200 m elevation, which are classified as Lower and we have heard and observed individuals of this Montane Very Wet Forest (Holdridge 1967). We species simultaneously with G. urraoensis. suspect that the species might range down to 2000 m, the lower elevational limit of this life zone in the Diet and foraging.- The diet of G. urraoensis region. Temperature in these forests ranges from 10 presumably consists largely of small- and medium- to 15ºC; annual rainfall averages 2044 mm and is sized invertebrates captured on the ground. Stomach bimodally distributed, with dry periods during the contents of specimens included only insect remains, first months of the year (Velásquez-Ruiz 2005). among which we were able to identify fragments of Canopy height is 8-10 m along forest edges and 12- coleopteran legs and wings. The species has also 15 m in forest interior. Forests are characterized by been observed foraging on earthworms captured in high relative humidity and a high diversity of the leaf litter. Earthworms are probably important epiphytes. The most common tree species are Quer- food items for nestlings, and we once observed an cus humboldtii (Fagaceae), Blakea longipes individual carrying several of them to feed its (Melastomataceae), Ocotea callophylla and Persea offspring (see section on reproduction below). sp. (Lauraceae), and Weinmannia sp. While foraging on the ground, G. urraoensis were (Cunnoniaceae); Podocarpus oleifolius observed removing leaf litter and soil with their feet (Podocarpaceae) occurs in the more pristine areas. as they searched for prey. After catching prey, birds Dominant plants in the middle stratum of the forest move their heads vigorously, often beating prey include tree ferns (Cyathea caracasana, Cya- against the ground and breaking items into pieces theaceae) and species of Schefflera and Oreopanax before ingesting them. (Araliaceae). Common plant families in the understory are Rubiaceae, Ericaceae, Araceae, and Reproduction.- Breeding in G. urraoensis appears Poaceae, with the bamboo Chusquea cf. scandens to concentrate in the earlier part of the year. The two being the most abundant species (Fig. 5). The new males we collected (one in February, the other in species is relatively common in primary and March) had large gonads, suggesting they were in secondary forests with these characteristics. It seems 66 New species of Grallaria from Colombia Carantón-Ayala & Certuche-Cubillos to prefer microhabitats where the understory is Frontino: Reserva Natural Colibrí del Sol dense, with a high abundance of epiphytes and (Fundación ProAves) and Reserva Forestal bamboo. Protectora Urrao-Abriaquí. Forests of this area have been badly disturbed below 2400 m, where now The full extent of the geographic distribution of G. limited to small, dispersed patches in an agricultural urraoensis is unknown, but based on the distribution and cattle-raising matrix. From 2400 to 2700 m, of seemingly suitable habitats, we suspect the forests are moderately disturbed; the landscape species might exhibit a continuous distribution in includes forests interspersed with some pastures and the northern sector of the Cordillera Occidental second-growth patches. At higher elevations, forests (Fig. 6). We suggest that additional possible are more continuous and have seen little human localities are the Nudo de Paramillo (departamento intervention. However, clearings on the steeper Antioquia), and Cerro Plateado, Farallones de slopes are frequent owing to treefalls and landslides. Citará, and Cerro Caramanta (Antioquia-Chocó Conservation of natural habitats in part of this area border). With knowledge of its distinctive voice, is enhanced by the purchase of 582 ha by Fundación confirming whether the species occurs at those sites ProAves. On the other hand, the Reserva Forestal should be relatively easy and would allow a better Protectora Urrao-Abriaquí (CORPOURABA) understanding of its distribution and conservation encompasses 32,000 ha purchased in 1975 to protect status (see below). Andean forest, paramo habitats, and water sources, but this reserve is not being continuously overseen. Conservation.- Premontane and montane forests in We suspect that G. urraoensis might also occur in the northern sector of the Cordillera Occidental have the northeast sector of Parque Nacional Natural Las been seriously affected by the creation of pastures Orquídeas, in the area known as Cerro Pelado. Since for cattle raising, agriculture, timber extraction, and 2004, the Colombian national park service hunting. Part of Páramo de Frontino is privately (UAESPNN, Territorial Noroccidental) has owned, and many areas have seen the expansion of proposed to extend this national park, currently cattle raising activities to steep slopes and the encompassing 32,000 ha, to include Páramo de general replacement of native forests by pastures. Frontino and surrounding areas, extending it to On gentler slopes, plantations of food crops 61,000 ha. However, effective conservation over including beans, passionfruit and tree tomato are such an extended area will require substantial frequent in the region. In addition, the area around investment in resources as well as alliances between Páramo de Frontino is known to maintain mineral public, private, and local organizations and deposits that include zinc, copper, and gold; this has communities. Fundación ProAves has promoted attracted the attention of mining companies, but alliances with CORPOURABA, the UAESPNN and owing to political instability in the area, active local authorities in Urrao, hoping to expand exploitation has not yet been undertaken. However, conservation areas to ensure the persistence of G. despite these mounting threats, the Frontino area urraoensis and other threatened species of plants remains in generally good condition from a and animals in the region. conservation perspective. This area comprises perhaps the best-conserved oak forests in the Based on the available information, it appears that Western Andes, well-conserved mixed forests and at G. urraoensis is seriously threatened by extinction higher elevations, and extensive paramo habitats owing to its restricted geographic distribution and supporting healthy populations of endemic plants likely small population size. We thus recommend such as Espeletia frontinoensis and Puya antioquen- that this species be listed as Critically Endangered sis. In addition, the area supports the only Polylepis according to IUCN criteria B1 a+b (i, ii, iii), known (i.e. Polylepis quadrijuga) forests found in Antio- range smaller than 100 km² (Critical); and C2a, quia, and represents the northwestern limit of this known population < 250 individuals (Critically genus, an iconic component of the High Andean Endangered). We believe that priority conservation vegetation. actions are establishing new protected areas and enforcing effective conservation in those where the There are only two protected areas in the Páramo de species occurs, in addition to searching for it in Ornitología Colombiana No. 9 (2010) 67
A. B.
Figure 5. Typical habitat in the Páramo de Frontino, Antioquia Colombia, where Grallaria urraoensis sp. nov. was discovered. A. Humid montane forest of Paramo de Frontino. B. View of the undergrowth at the type locality. Farallones de Citará and Cerro Plateado. Such surveys could result in increased knowledge of the distribution and population sizes of the new species, and of the distribution and status of other threatened and little-known birds occurring in the region such as Dusky Starfrontlet, Rusty-faced Parrot (Hapalopsittaca amazonina), Moustached Antpitta (Grallaria alleni), and Chestnut-bellied Flowerpiercer.
ACKNOWLEDGMENTS
We are especially grateful to C. D. Cadena, who offered valuable assistance and help with translation, and made many editorial changes and valuable comments on the manuscript; this description would not have been possible without his support. We also thank the staff of research and conservation of Fundación ProAves (in particular A. Paez, A. Quevedo, H. Valle, and M. I. Moreno) with support from American Bird Conservancy and USFWS Neotropical Migratory Bird Conservation Act. We are grateful to CORPOURABA (especially Figure 6. Map of southwest Antioquia, showing the type local- ity (Páramo de Frontino) of the Urrao Antpitta (Grallaria urra- H. Doria) and Unidad Administrativa Especial de oensis sp. nov.) and the distribution of Andean forests and pa- Parques Nacionales Naturales (Parque Las ramo vegetation in the Western Andes of Colombia. Map based Orquídeas) for providing research permits and on SIRAP Antioquia (Anonymous 2007). collaboration. L. R. García, F. Jiménez, H. Velásquez, and A. Duque provided help and logistic other areas where it might be found. To this latter support, and we appreciate the kind hospitality of end, we suggest that searches for new populations the local people of Urrao. Members of the Grupo de should focus from Páramo de Frontino north to the Observadores de Aves del Tolima (GOAT), M. Nudo de Paramillo (Antioquia) and south to Cerro Moreno, B. Florido, C. Díaz, J. Sanabria, A. Lugo, Tatamá (Risaralda), with particular attention to the and L. Guerrero, provided advice and support. F. G. 68 New species of Grallaria from Colombia Carantón-Ayala & Certuche-Cubillos
Stiles offered valuable assistance with the C UERVO , A. M., P. C. PULGARÍN & D. CALDERÓN. description and curation of the type series at the 2008. New distributional bird data from the ICN, and provided helpful comments on the Cordillera Central of the Colombian Andes, with manuscript. We also thank S. Sierra, F. Forero and implications for the biogeography of M. Álvarez (IAvH), H. Álvarez-López (Universidad Northwestern South America. Condor 110:526- del Valle), and W. Múnera and P. Pulgarin 537. (Universidad del Antioquia) for allowing us to C UERVO, A. M., F. G. STILES, C. D. CADENA, J. L. examine specimens in their care. C. A. Rojas TORO & G. A. LONDOÑO. 2003. New and assisted in preparing the map. The Facultad de noteworthy bird records from the northern sector Ciencias of the Universidad del Tolima provided of the Western Andes of Colombia. Bulletin of technical and logistic support. This manuscript was the British Ornithologists' Club 123:7-24. improved thanks to discussions with R. Sedano and FLÓREZ, P., N. KRABBE, J. CASTAÑO, G. SUÁREZ & Y. G. Molina. M. Robbins and J.V. Remsen J. D. ARANGO. 2004. Evaluación avifauna del provided valuable comments on the manuscript. Páramo de Frontino, Antioquia, Agosto 2004. Colombian EBA Project Report Series No. 6, LITERATURE CITED Fundación ProAves, Bogotá, Colombia. FUNDACIÓN PROAVES[online].2009. Informe anual ANONYMOUS. 2007. Informe de Consolidación de la ProAves 2008.
KRABBE, N. & P. COOPMANS. 2000. Rediscovery of Andes of Colombia. Ornitología Colombiana 1: Grallaria alleni (Formicariidae) with notes on its 4-21. range, song and identification. Ibis 142:183-187. SALAMAN, P., T. M. DONEGAN & R. PRŶS-JONES. KRABBE, N., P. FLÓREZ, G. SUÁREZ, J. CASTAÑO, J. 2009. A new subspecies of Brown-banded D. ARANGO & A. DUQUE. 2006. The birds of Antpitta Grallaria milleri from Antioquia, Páramo de Frontino, Western Andes of Colombia. Bulletin of the British Ornithologists' Colombia. Ornitología Colombiana 4:39-50. Club 129:5-16. KRABBE, N., P. FLÓREZ, G. SUÁREZ, J. CASTAÑO, J. SALAMAN, P. G. W., L. MAZARIEGOS, M. D. M. D. ARANGO, P. C. PULGARÍN, W. A. MÚNERA, F. OLIVES & L. M. RENJIFO. 2002. Eriocemis G. STILES & P. SALAMAN. 2005. Rediscovery of mirabilis. Pages 264-266 in: L. M. Renjifo, A. the Dusky Starfrontlet Coeligena orina, with a M. Franco-Maya, J. D. Amaya-Espinel, G. H. description of the adult plumages and a Kattan, and B. López-Lanús (eds.). Libro rojo de reassessment of its taxonomic status. Ornitología aves de Colombia. Instituto Alexander von Colombiana 3:28-35. Humboldt & Ministerio del Medio Ambiente, KRABBE, N. & T. S. SCHULENBERG. 2003. Family Bogotá, Colombia. Formicariidae (Ground-Antbirds). Pages 682-731 SALAMAN, P. G. W. & F. G. STILES. 1996. A in Handbook of the birds of the world, volume 8: distinctive new species of vireo (Passeriformes: broadbills to tapaculos (J. del Hoyo, A. Elliott, Vireonidae) from the Western Andes of and D. Christie, Eds.). Lynx Edicions, Barcelona. Colombia. Ibis 138:610-619. LOWERY, G. H. J. & J. P. O'NEILL. 1969. A new SCHULENBERG, T. S. & M. D. WILLIAMS. 1982. A species of Grallaria from Peru, and a revision of new species of antpitta (Grallaria) from northern the subfamily Grallarinae. Auk 86:1-12. Peru. Wilson Bulletin 94:105-113. PUEBLA-OLIVARES, F., E. BONACCORSO, A. S MITHE , F. 1975, 1981. Naturalists' color guide. ESPINOSA DE LOS MONTEROS, K. E. OMLAND, J. American Museum of Natural History Press, E. LLORENTE-BOUSQUETS, A. T. PETERSON & A. New York. G. NAVARRO-SIGÜENZA. 2008. Speciation in the STILES, F. G. 1992. A new species of antpitta Emerald Toucanet (Aulacorhynchus prasinus) (Formicariidae: Grallaria) from the Eastern complex. Auk 125:39-50. Andes of Colombia. Wilson Bulletin 104:389- PULGARÍN-R., P. C. & W. A. MÚNERA-P. 2006. 399. New bird records from Farallones del Citará, TORO, J. L. 2002. Diglossa gloriossisima in Libro Colombian Western Cordillera. Boletín SAO rojo de aves de Colombia. Serie Libros Rojos de 16:44-53. Especies Amenazadas de Colombia (L. M. RENJIFO, L. M., A. M. FRANCO-MAYA, J. D. Renjifo, A. M. Franco-Maya, J. D. Amaya- AMAYA-ESPINEL, G. H. KATTAN & B. LÓPEZ- Espinel, G. H. Kattan, and B. López-Lanús, LANÚS (EDS.). 2002. Libro rojo de aves de Eds.). Instituto de Investigación de Recursos Colombia. Instituto Alexander von Humboldt & Biológicos Alexander von Humboldt & Ministerio del Medio Ambiente, Bogotá, Ministerio del Medio Ambiente, Bogotá, Colombia. Colombia. ROBBINS, M. B. & F. G. STILES. 1999. A new T ORO, J. L. & P. FLÓREZ. 2001. Una nueva pobla- species of Pygmy-Owl (Strigidae: Glaucidium) ción del Loro Orejiamarillo (Ognorhynchus from the Pacific slope of the Northern Andes. icterotis) en los Andes de Colombia. Boletín The Auk 116:305-315. SAO 12:47-51. SALAMAN, P., P. COOPMANS, T. M. DONEGAN, M. VELÁSQUEZ-RUIZ, C. A. 2005. Paleoecología de alta MULLIGAN, A. CORTÉS, S. L. HILTY, AND L. A. resolución del Holoceno Tardío en el Páramo de ORTEGA. 2003. A new species of wood-wren Frontino Antioquia. Universidad Nacional de (Troglodytidae: Henicorhina) from the Western Colombia, Sede Medellín. Medellin.
Recibido: 19 enero 2010 Aceptado: 06 mayo 2010 70 New species of Grallaria from Colombia Carantón-Ayala & Certuche-Cubillos
Appendix 1. Localities and specimens of Grallaria examined at the Instituto de Ciencias Naturales (ICN-MHN), Bogotá, Colombia; Instituto de Investigación en Recursos Biológicos Alexander von Humboldt (IAVH), Villa de Leyva, Colombia; Colección Ornitológica de la Universidad del Valle, Cali, Colombia, and Museo Universitario de Antioquia MUA-AVP.
Grallaria milleri: ICN-MNH 36692, Vereda Palomas, Reserva Natural Río Blanco, Caldas, Col., 2650 m, female; IAvH 13203, Berlin, Pensilvania, Caldas, Col., 2750 m, female; IAvH 13205, Berlin, Pensilvania, Caldas, Col., 2750 m, male; UVC 6171, Parque Regional Ucumarí, La Pastora, Pereira, Risaralda, Col., 2400 m, male; UVC 6178, Parque Regional Ucumarí, La Pastora, Pereira, Risaralda, Col., 2400 m, female; UVC 6179, Parque Regional Ucumarí, La Pastora, Pereira, Risaralda, Col., 2400 m, male; UVC 6180, Parque Regional Ucumarí, La Pastora, Pereira, Risaralda, Col., 2400 m, male; UVC 6181, Parque Regional Ucumarí, La Pastora, Pereira, Risaralda, Col., 2400 m, male; UVC 6182, Parque Regional Ucumarí, La Pastora, Pereira, Risaralda, Col., 2400 m, male. Grallaria kaestneri: ICN-MHN 30731, Monterredondo Camino de San Juanito, Guayabetal, Cundinamarca, Col., 2300 m, Female; ICN-MHN 36310, Monterredondo, Guayabetal, Cundinamarca, Col., 2300 m, chick. Grallaria rufocinerea: IAvH 0525, Rio Bedón, PNN Puracé, Col., male; IAvH 0526, Rio Bedón, PNN Puracé, Col. Grallaria nuchalis: IAvH 13235, Berlin, Pensilvania, Caldas, Col., 2750, male. Grallaria hypoleuca: ICN-MHN 11842, La Candela, Huila, Col., 1600 m, female; ICN-MHN 35552, San Isidro, Galán, Santander, Col., 1995 m, female; IAvH 6566 Virolín, Charalá, Santander, Col., male. Grallaria quitensis: ICN-MHN 33381, Distrito Capital, Laguna Bocagrande, Macizo Sumapaz, Cundinamarca, Col., 3600 m, female; ICN-MNH 22973, Nevado la Cueva, Guicán, Boyacá, Col., male; IAvH 2488, Pilimbala, PNN Puracé, Cauca, Col., 3380 m, female; IAvH 6805, Finca Indostan, Anzoátegui, Tolima, Col., male. Grallaria rufula: ICN-MHN 11815 San Miguel, Cundinamarca, Col., male; ICN-MHN 11816, Páramo de Guasca, Col., female; ICN-MHN 23549, San Pedro, Cuchilla Cebolleta, Sierra Nevada de Santa Marta, Col., 2500 m, male; ICN-MHN 31324, Junín, Carpanta, Cundinamarca, Col., 2600 m; IAvH 2436, Quilindos, Santa Cecilia, Cauca, Col., 3020 m, female; IAvH 6631, PNN Chingaza, Cundinamarca, Col., female; IAvH 13358, PNN Tatamá, Pueblo Rico, Risaralda, 2680 m, female; MUA-AVP 0556, Finca La Martinica, Distrito siete, Vereda Desquite, Manizales, Caldas, Col. Grallaria ruficapilla: IAVH 11928, Vereda el Laurel, Aranzazu, Caldas, Col., 2250 m, male. Grallaria guatimalensis: ICN-MHN 33287, Puerto Leguízamo, Putumayo, Col., male; MUA-AVP 198, Medellín, Antioquia, Col. Grallaria haplonota: ICN-MHN 31182, Alto de Pisones, 8 km al norte of Geguadas, Mistrató, Risaralda, Col., 1620 m, male. Grallaria alleni: IAvH 10741, SFF Otún Quimbaya, Risaralda, Col., 1800 m, male.
Appendix 2: Records and localities of vocalizations of Grallaria examined. XC refers to www.xeno-canto.org catalogue numbers. IAvH-BSA refers to Instituto de Investigación de Recursos Biológicos Alexander von Humboldt ’s sound archive catalogue numbers.
Grallaria milleri: Reserva Natural El Mirador, Génova, Quindío, Colombia, 2670 m, (Nick Athanas: XC 10721); Reserva Natural Río Blanco, Caldas, Colombia, 2650 m, (Bradley Davis: XC 13896); Reserva Natural El Mirador, Génova, Quindío, Colombia, 2700 m, (Frank Lambert: XC 16777); Reserva Natural Río Blanco, Caldas, Colombia, 2600 m, (David Bradley: XC 17619); Reserva Natural Río Blanco, Caldas, Colombia, 2800 m, (Hernan van Oosten: XC 18289), Reserva Natural Río Blanco, Manizales, Caldas, Colombia, 2400 m, (Oswaldo Cortés: XC 20505); Reserva Natural Río Blanco, Caldas, Colombia, 2800 m, (Andrew Spencer: XC 22213); Reserva Natural Ibanasca, Juntas, Ibagué, Tolima, Colombia N 04°25’ W 75°12’, (Oscar Laverde: IAvH-BSA 24192); Reserva Natural Ibanasca, Juntas, Ibagué, Tolima, Colombia N 04°25’ W 75° 12’ (Mauricio Alvarez R: IAvH-BSA 22433); Reserva Natural Río Blanco, Manizales, Caldas, Colombia, N 05°05’ W 75°21’, (Diego Calderón F & Fundegar: IAvH-BSA 22767). Grallaria kaestneri: Monterredondo, Cundinamarca, Colombia, 2100 m (Hernan van Oosten: XC 17990); Monterredondo, Cundinamarca, Colombia, 2100 m (Hernan van Oosten: XC 17991); Monterredondo, Cundinamarca, Colombia, 2100 m (Hernan van Oosten: XC 17992); Farallones de Medina, Cundinamarca, Colombia, 2000 m, (Oswaldo Cortés, John King & Jürgen Beckers: XC 18599); Farallones de Medina, Cundinamarca, Colombia, 2000 m, (Oswaldo Cortés, John King & Jürgen Beckers: XC 18600); Farallones de Medina, Cundinamarca, Colombia, 2000 m, (Oswaldo Cortés, John King & Jürgen Beckers: XC 18601), Farallones de Medina, Cundinamarca, Colombia, 2000 m, (Oswaldo Cortés, John King & Jürgen Beckers: XC 18602); Cundinamarca, Colombia, 2100 m, (Oswaldo Cortés: XC 20323); Cundinamarca, Colombia, 2100 m, (Oswaldo Cortés: XC 20324); Cundinamarca, Colombia, 2100 m, (Oswaldo Cortés: XC 20325); Cundinamarca, Colombia, 2100 m, (Oswaldo Cortés: XC 20326); Cundinamarca, Colombia, 2100 m, (Oswaldo Cortés: XC 20327).